Chem Soc Rev

View Article Online TUTORIAL REVIEW View Journal | View Issue

Phosphorus recovery and recycling – closing the loop† Cite this: Chem. Soc. Rev.,2021, 50,87 Andrew R. Jupp, ‡*ab Steven Beijer,‡a Ganesha C. Narain,a Willem Schipperc and J. Chris Slootweg *a

There is a clear and pressing need to better manage our planet’s resources. Phosphorus is a crucial element for life, but the natural phosphorus cycle has been perturbed to such an extent that humanity faces two dovetailing problems: the dwindling supply of phosphate rock as a resource, and the overabundance of phosphate in water systems leading to eutrophication. This Tutorial Review will explore the current routes to industrial phosphorus compounds, and innovative academic routes towards accessing these same products in a more sustainable manner. It will then describe the many Received 4th September 2020 ways that useful phosphate can be recovered from waste streams, and how it can be recycled and used DOI: 10.1039/d0cs01150a as a resource for new products. Finally, we will briefly discuss the barriers that have thus far prevented

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. the widespread adoption of these technologies, and how we can close the loop to establish a modern rsc.li/chem-soc-rev phosphorus cycle.

Key learning points (1) Why is phosphorus important and how has the natural phosphorus cycle been disrupted? (2) How are phosphorus-containing compounds currently synthesized? (3) Can these same products be accessed in more environmentally friendly and sustainable ways? (4) How can phosphorus be recovered and recycled?

This article is licensed under a (5) What barriers need to be overcome to re-establish the phosphorus cycle? Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. Introduction weapon in warfare, both as an incendiary agent and for creating smoke screens. Despite these nefarious uses, phosphorus is 2019 marked the 350th anniversary of the discovery of one of also an element that is essential to all known forms of life. the periodic table’s most beguiling and multifaceted elements. Phosphorus is most commonly found in nature in its highest Phosphorus was first discovered in 1669 by Hennig Brand, an oxidation state (+5). Phosphorus is required for the formation alchemist from Hamburg, who heated the malodorous residues of nucleotides, which comprise DNA and RNA molecules, and is of urine with sand and coal in a quest for the ‘‘philosopher’s a crucial component of ATP (adenosine triphosphate), which is stone’’.1,2 The substance he isolated gave off a pale green glow, the primary energy carrier in cells. Furthermore, phospholipid and he thus named it phosphorus, from the Greek for light- bilayers are found in the membranes of cells, and calcium bearer. We now know that Brand had isolated white phos- phosphate is the primary component of mammalian bones and

phorus, an elemental allotrope that consists of discrete P4 teeth. The essential nature of phosphorus combined with its tetrahedra. White phosphorus was originally (and misguidedly) relatively low abundance compared to other essential nutrients sold as a medicine for a wide range of ailments, but the has led to the element being dubbed ‘‘life’s bottleneck’’ by Isaac 3 pyrophoric nature of P4 resulted in its subsequent use as a Asimov. The natural phosphorus cycle, which has been established a Van ‘t Hoff Institute for Molecular Sciences, University of Amsterdam, P.O. Box over geological timescales, first involves the weathering of 94157, 1090 GD Amsterdam, The Netherlands. E-mail: [email protected] phosphorus-containing minerals into soil and streams. From b School of Chemistry, University of Birmingham, Edgbaston, Birmingham, B15 2TT, here it is taken up by microbes and plants, and subsequently by UK. E-mail: [email protected] c Willem Schipper Consulting, Oude Vlissingseweg 4, 4336 AD, The Netherlands animals that eat the plants, and used to promote growth. The † Electronic supplementary information (ESI) available. See DOI: 10.1039/d0cs01150a phosphorus returns to the soil via excretion from animals ‡ These two authors contributed equally. during their lifetime, and by decomposition of plants and

This journal is © The Royal Society of Chemistry 2021 Chem. Soc. Rev.,2021,50,87--101 | 87 View Article Online Tutorial Review Chem Soc Rev

animals after death, where it can be taken up again by living shown historical ebbs and flows,4 but given the long timelines creatures. This part of the process, the phosphate being taken involved nature has always managed to redress this balance. up by animal and plant life and subsequently returned to the This natural equilibrium has been severely impacted by soil, can be repeated numerous times. Over time, some phos- human activity.5 Deforestation, and the associated soil loss, phorus is lost to waterways and eventually the sea, where over has led to more rapid loss of phosphate from the ground into long periods of time it is reincorporated in sedimentary rock. surface waters. Furthermore, phosphate-based fertilizers have Like most natural cycles, the phosphorus cycle has not neces- been required to feed an ever-growing global population, and sarily remained completely constant over time; studies have this has required extensive mining of phosphate rock (PR);

Andrew Jupp obtained his PhD Steven Beijer obtained his BSc in from the University of Oxford chemistry at Utrecht University (2012–2016) under the super- and his MSc at the University of vision of Prof. Jose Goicoechea. Amsterdam with an emphasis on He worked on phosphorus analo- energy and sustainability. His gues of the cyanate anion and master’s thesis on valorizing phos- urea, for which he was awarded phate from waste streams was the Reaxys PhD Prize in Hong awarded the Unilever Research Kong in 2015. He subsequently Prize 2019. He is currently a PhD carried out a Banting Post- candidate under the supervision doctoral Fellowship with Prof. of Assoc. Prof. Chris Slootweg. Doug Stephan at the University His research focuses on the Creative Commons Attribution-NonCommercial 3.0 Unported Licence. Andrew R. Jupp of Toronto (2016–2018), working Steven Beijer sustainable use of phosphorus, on the synthesis and reactivity of positioning him at the inter- main-group Lewis acids and bases, and the functionalisation of section of developing novel recycling methodologies and exploring carbon dioxide. In 2018, he became an NWO VENI laureate at the their potential for large-scale implementation. University of Amsterdam, working with Assoc. Prof. Chris Slootweg on the formation of main-group radicals. In 2020, he launched his independent career as a Birmingham Fellow at the University of Birmingham (UK), working on small-molecule activation and

This article is licensed under a molecular photo-switches.

Ganesha (Nesha) Narain obtained Willem Schipper received his MSc Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. his Master’s degree in Chemistry in 1989 and his PhD in 1993, at from the University of Amsterdam Utrecht University in physical and the Vrije Universiteit chemistry under the supervision Amsterdam. He worked on of Prof. G. Blasse. He subse- phosphorus recovery and quently joined Hoechst Holland, recycling and molecular sensing. which later became Thermphos His focus has been sustainability, International, as chemist sup- circular economy and renewable porting the industrial production energy. He obtained his of white phosphorus and Bachelor’s degree in Chemical phosphates. As Senior Chemist, Engineering from the University he pioneered the use of secondary Ganesha C. Narain of Twente focusing on material Willem Schipper raw materials, such as sewage engineering and a research into sludge ash and meat and bone photocatalytic water splitting. Nesha is currently pursuing a career meal ash, for the production of white phosphorus. As Innovation as a strategy consultant. He remains a sustainability enthusiast Manager he explored the direct functionalisation of white and keeps aiming for societal impact. phosphorus to obtain various phosphorus containing chemicals, bypassing the existing derivatives routes, and developed the synthesis and chemistry of phosphorus trioxide. Since 2013 he works as independent consultant to the industry and the scientific world, focusing on recycling, phosphorus chemistry, and process development.

88 | Chem. Soc. Rev.,2021,50,87--101 This journal is © The Royal Society of Chemistry 2021 View Article Online Chem Soc Rev Tutorial Review

approximately 20 Mt P is annually extracted from the earth.6 This is problematic because PR is a finite and dwindling resource. Furthermore, it is not equally distributed around the globe, with three quarters of the supply found in Morocco and Western Sahara, and other significant quantities in China, the USA and Russia. This asymmetric distribution of such an essential resource, combined with its economic volatility (the price of phosphorus briefly increased eightfold in 2008) could lead to sensitive food security situations and future political tensions.7 An accurate value of total useful reserves of PR is hard to predict, since this is highly dependent on the price. When the price increases, currently uneconomic reserves may become economically viable. Furthermore, when there is scar- city, the incentive to search for new reserves is higher. Due to this uncertainty, the estimates for depletion of PR reserves range from 40 to 400 years.8 The increased amount of phosphate in the soil from fertili- zers and animal excrement also leads to an inevitable increase in the loss of phosphates into waterways. This is not merely wasteful; it has led to anthropogenic eutrophication, which is the process where the increased phosphate content leads to enormous blooms of algae, which depletes the water of oxygen 9

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. and decimates marine ecosystems. It is apparent that the geological formation of PR from this run-off is negligible compared to the last century’s intensive use of fertilizers and phosphate-based feed and food additives, and the phosphorus cycle is no longer a cycle; it is instead an unequivocally linear process. There is therefore a problem of not enough phosphorus, Fig. 1 Schematic representation of the natural and anthropogenic phos- with the dwindling supply of accessible PR, and of too much phorus cycles. phosphorus in our surface waters leading to environmental This article is licensed under a concerns. These dovetailing problems necessitate the need for efficient phosphorus recovery and recycling schemes, which are This Tutorial Review will first look at current industrial essentially replacing the geological regeneration of PR on a routes to phosphorus-containing products, followed by relevant timescale relevant to the human-disrupted phosphorus cycle and sustainable routes to similar compounds that have been Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. (Fig. 1). demonstrated on a laboratory, pilot or industrial scale. We will then explore the various ways phosphate can be recovered and recycled, followed by the barriers and obstacles to fulfilling this goal of closing the loop on the modern phosphorus cycle.10 Chris Slootweg was born in Haarlem (The Netherlands) in 1978 and received his Traditional routes to phosphorus and undergraduate education from phosphates Vrije Universiteit Amsterdam in 2001. After earning his PhD in The phosphorus required for industrial processes is traditionally 2005 under the supervision of obtained by mining PR. This consists mainly of apatite:

Prof. Koop Lammertsma, he Ca5(PO4)3X, (X = OH, F, Cl), with fluoroapatite (Ca5(PO4)3F) the pursued postdoctoral studies at most common. There is often a high degree of isomorphic the ETH Zu¨rich with Peter Chen. substitution of carbonate ions for phosphate ions in naturally In 2006, he returned to VU to occurring PR as well, depending on geographical location. Over initiate his independent career. 80% of mined phosphorus comes from sedimentary PR, which has J. Chris Slootweg He was promoted to Associate a relatively high phosphate content (reported by convention as 11,12 Professor in 2014, and moved to phosphorus pentoxide content) of up to 40% P2O5. However, the University of Amsterdam in 2016. The mission of his laboratory the sedimentary deposits can contain a wide range of pollutants is to educate students at the intersection of fundamental physical and heavy metal contaminants, including radioactive metals such organic chemistry, main-group chemistry, and circular chemistry. as uranium and thorium. Depending on the requirements of

This journal is © The Royal Society of Chemistry 2021 Chem. Soc. Rev.,2021,50,87--101 | 89 View Article Online Tutorial Review Chem Soc Rev

subsequent steps and the final product, these impurities can be the transfer of the phosphoric acid from the aqueous phase to removed by subsequent treatment, often by precipitation or extrac- an organic phase (such as methyl isobutyl ketone or tributyl tion. Igneous rock deposits typically have lower levels of radioactive phosphate), while the majority of the impurities remain in impurities, but also much lower phosphorus concentrations the aqueous phase.15 Cationic impurities can be removed by

(0.005–2% P2O5). Fortunately, beneficiation methods (mechanical adding sulfuric acid to form sulfate salts, which remain in separation of minerals, usually involving grinding and flotation) the aqueous phase. The extraction methods do not work for 11 can yield PR with 35–40% P2O5 content. There are some meta- arsenic and cadmium impurities, so precipitation methods are

morphic rock deposits that contain 0.01–1.3% P2O5,buttheseare required. Arsenic can be separated by adding sodium sulfide, often deep-lying and not very porous, which makes subsequent which leads to precipitation of arsenic sulfide, while cadmium treatment more difficult, and as such these deposits are not yet can be removed using complexing agents such as dialkyldithio- 16 economically viable. Seabed phosphate deposits are currently phosphoric acid esters (S = P(SH)(OR)2). If desired, cationic being explored in Namibia and Mexico, illustrating the ongoing impurities (Fe, Al, Mg and Ca) can be removed by neutralizing quest for finding new exploitable PR reserves. After mining, the PR the acid with sodium hydroxide, resulting in a mixed mono/ is ground and treated via the wet or thermal processes. disodium phosphate solution and the precipitation of metal hydroxides. However, this method is limited by the fact that the Wet process phosphoric acid is transformed to phosphate salts only usable The vast majority of PR, about 98% of it, is processed via the for products such as detergents. wet process to yield wet phosphoric acid.6 This process consists of acidulation followed by concentration and purification Thermal process (precipitation and extraction). The acidulation is generally The thermal (or Wo¨hler) process is an energy intensive process

performed with sulfuric acid (H2SO4) to afford phosphoric acid that produces elemental white phosphorus (P4). The remaining (H3PO4) and the by-products phosphogypsum (various hydrates 2% of mined PR is processed this way. The chemical reaction is

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. of CaSO4) and hydrogen fluoride (HF) according to eqn (1): actually remarkably similar to that in Hennig Brand’s urine- boiling quest for the philosopher’s stone, and involves the Ca5(PO4)3F+5H2SO4 +5nH2O - 3H3PO4 + 5CaSO4ÁnH2O heating of PR with coke (carbon) and silica (SiO2; for CaSiO3 +HF(n = 0, 0.5 or 2) (1) slag formation) to temperatures of 1500–1600 1C according to eqn (2). Roughly five tons of phosphogypsum are produced per ton 13 - of phosphoric acid. Phosphogypsum is mostly landfilled 4Ca5(PO4)3F + 18SiO2 + 30C 3P4 + 30CO + 18CaSiO3 + 2CaF2 (88%) or disposed at sea (10%) and requires careful deposit (2) management such as containment and treatment of drainage This article is licensed under a water to avoid environmental problems; only a small amount of The coke acts as a reducing agent to give diphosphorus gas

gypsum is used as raw material (o2%). Recent work has shown (P2 – the heavier congener of dinitrogen), which dimerises and that valuable rare earth elements can be recovered from the condenses to white phosphorus. The process has a large energy

phosphogypsum waste, allowing the remaining material to consumption of 12.5–14 MW h per tonne of P4 produced, but Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. be used as an alternative to natural gypsum in cements or gives a relatively pure product that can be functionalised to a plasterboards.14 large range of phosphorus-containing chemicals (see Fig. 2).11

To prevent the formation of phosphogypsum, the acidulation The market value of P4 and its primary derivatives is estimated can be carried out using nitric acid, which yields marketable at several billion USD yÀ1.6 A significant part of the global calcium nitrate as the by-product. However, the cost of nitric acid supply of white phosphorus is oxidised to phosphorus pent-

is higher than sulfuric acid, so only 10% of the wet process carried oxide (P4O10) and subsequently hydrolysed to afford high-purity out worldwide is performed with nitric acid.15 Hydrochloric acid thermal phosphoric acid, which is (also as its sodium, calcium can also be used to obtain a relatively pure product, but this poses and potassium salt) suitable for use in foodstuffs, beverages, a separation challenge to remove calcium chloride, hence it is toothpaste and detergents. The latter use is declining, due to a chieflyoperatedinparallelwithasolventextractionsetupto ban of phosphates in detergents in several parts of the world to obtain purified phosphoric acid. help combat increasing levels of phosphates in water bodies. About 92% of the phosphoric acid is converted into The only significant impurity in this thermal phosphoric acid is fertilizers,6 representing a market valued at several tens of arsenic (5–30 ppm), which could arise from small amounts of À1 17 billion USD y . Many of the impurities from the PR, including AsP3 in the white phosphorus. The arsenic can be removed via the HF by-product, are still present in the phosphoric acid (and/ addition of sodium sulfide and precipitation of arsenic sulfide or the phosphogypsum by-product) depending on the type of (vide supra). digestion process and the origin of the PR. The impurities can Organophosphorus compounds, i.e. molecules featuring a be removed by several methods, most commonly extraction and P–C bond, or mixed P–C and P–O–C bonds, are found in many precipitation, which are chiefly used to produce feed- (5%), or bulk and specialty chemicals, such as flame-retardants, metal 6 technical- and food grade phosphates (3%); fertilizer grade extractants and pesticides. Phosphines, PR3, are a widely used acid is rarely treated to remove impurities. Extraction involves class of ligand to support homogeneous transition metal

90 | Chem. Soc. Rev.,2021,50,87--101 This journal is © The Royal Society of Chemistry 2021 View Article Online Chem Soc Rev Tutorial Review

alternatives to PCl3 for the synthesis of organophosphorus

compounds. Phosphine gas, PH3, is used on industrial scales to synthesise organophosphorus compounds, although it is itself highly toxic and pyrophoric (the latter on account of trace

P2H4 impurities). Phosphinate esters, also called hypopho- sphites (H2P(O)(OR)), and sodium hypophosphite (NaH2PO2), have also been explored in the formation of organophosphorus compounds via P–C bond formation by hydrophosphinylation of alkenes and alkynes.21 In particular, sodium hypophosphite is used in the synthesis of aluminium diethyl phosphinate, which is produced industrially as a flame-retardant (Fig. 3A).22

To circumvent the use of a PCl3 surrogate at all, the direct functionalisation of white phosphorus has been researched in

earnest since the 1970s. The reactivity of the P4 tetrahedron, usually attributed to the inherent ring strain, is difficult to control, with nucleophilic, electrophilic, and radical pathways sometimes operating concurrently. A large range of phosphorus-

containing products have been synthesised from P4; this topic has

been reviewed extensively, with reviews focusing on P4 activation by transition metals, main-group systems and via electrocatalytic functionalization, and will not be further discussed here.23 White phosphorus is the most reactive allotrope of phosphorus, so

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. Fig. 2 Use of phosphorus in the chemical industry, with precursors to efforts to use more benign red phosphorus as an alternative to

organophosphorus compounds highlighted. PCl3 necessitate more forcing conditions. Red phosphorus, which is formed by heating white phosphorus to 250 1C, has a chain-like polymeric structure, and is used as-is in matchboxes and flame- catalysts, as a key component of Wittig reactions (see below), retardants, but is not relevant as a separate raw material for and over the last decade have been explored as part of frustrated follow-up chemistry. In fine chemicals synthesis on lab or small Lewis pairs for small molecule activation and metal-free industrial scale, red phosphorus is reduced using alkali metals to hydrogenations.18 The vast majority of organophosphorus com- form highly reactive metal phosphides (M3P;M=Li,Na,K).These pounds are industrially synthesised using phosphorus trichloride are usually generated and functionalised in situ,oftenvia

This article is licensed under a (PCl3) as a precursor, which is generated in turn by the direct the protonated analogues (M2PH and MPH2), affording a diverse chlorination of white phosphorus. This process can also afford array of phosphines and phosphine oxides. As a representative other chlorinated derivatives, such as PCl5,PSCl3 and POCl3. Phosphorus trichloride can be functionalised using Grignard or

Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. organolithium reagents, or by reaction with halogenated organic compounds under forcing reducing conditions.19 They can also be converted to phosphonates (including glyphosate) in a modified Mannich reaction, or to a range of alkyl and aryl phosphites by treatment with alcohols in the presence of an amine to capture HCl.

Alternative routes to organophosphorus compounds

PCl3 is a very useful chemical synthon for the synthesis of organophosphorus compounds, but is not an ideal reagent in terms of sustainability and safety due to its inherent corrosive- ness, high toxicity and moisture sensitivity.20 It is a precursor on the list of Schedule 3 substances of the Chemical Weapons Convention, and thus its manufacture is carefully regulated. Moreover, very few of the final products contain a P–Cl bond,

so the use of the toxic chlorine gas to functionalise white Fig. 3 Selected examples of methods to synthesise organophosphorus

phosphorus can be regarded as a necessary yet wasteful step. compounds avoiding the use of PCl3. Mes = mesityl; OAc = acetate; Therefore, there has been a lot of research into finding TPPO = triphenylphosphine oxide; TMEDA = tetramethylethylenediamine.

This journal is © The Royal Society of Chemistry 2021 Chem. Soc. Rev.,2021,50,87--101 | 91 View Article Online Tutorial Review Chem Soc Rev

example, bis(mesitoyl)phosphinic acid, a water-soluble and stable (which can be converted to HSiCl3) can be formed directly from analogue of the commercially available photo-initiators known as orthosilicates.33 bis(acyl)phosphine oxides (BAPOs), was recently synthesised by Gru¨tzmacher and co-workers in a one-pot procedure from red phosphorus (Fig. 3B).24 Note, further processing of white or red Phosphorus recovery and recycling phosphorus can lead to other allotropes: violet phosphorus, which The examples of sustainable phosphorus chemistry mentioned consists of a polymer of alternating [P8]and[P9]unitslinkedby pairs of P atoms, and black phosphorus, which is a layered thus far are all innovative but are limited to linear processes (or structure of puckered six-membered rings.25 small self-contained cycles such as the TPP/TPPO recycling), There are examples of recycling of certain phosphorus and do not contribute significantly to closing the phosphorus compounds in small and self-contained cycles. The Wittig loop on a global scale. Awareness of the need to better manage reaction, named after the chemist who shared the 1979 Nobel the planet’s dwindling resources has increased exponentially Prize for Chemistry for its discovery, is used on an industrial over the recent decades, and there has been a growing effort 34 scale in the synthesis of vitamins and pharmaceuticals. In this towards developing a circular economy. This is particularly process, a phosphine (often PPh , TPP) is first converted to a relevant in the chemical sector and the principles of circular 3 35 phosphonium ylide, which reacts with an aldehyde or ketone to chemistry were recently outlined. The overarching idea is that generate the desired alkene and an equivalent of the by-product all waste should be collected and used, and this notion is gaining traction in the phosphorus industry. phosphine oxide (OPPh3, TPPO). The phosphine oxide is typically treated as waste. The chemical company BASF have developed a There are many phosphorus-containing waste streams that, large-scale recycling process for TPPO, which involves chlorina- if properly exploited, have the potential to replace a significant tion with phosgene and reduction with aluminium powder.26 portion of the phosphorus produced by traditional mining. Van Although these hazardous reagents and conditions do not comply Dijk et al. mapped out the phosphorus-containing streams in the EU-27 for the year of 2005.36 Of the total amount of

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. with all the tenets of green chemistry, the process is still more environmentally sustainable and cost effective than disposing of imported phosphorus in 2005, 51% was lost as waste, 39% accumulated in the soil and the remainder was exported. The the TPPO and having to synthesise new TPP from PCl3,sodium and chlorobenzene. Catalytic variants of the Wittig reaction have largest share (54%) of losses is from human consumption, of also been developed on a laboratory scale, using milder reducing which 55% was lost via wastewater. This loss of phosphorus into wastewater therefore amounts to 15% of the total imported agents such as diphenylsilane (Ph2SiH2), to convert the TPPO to TPP in situ,27 and electrochemical methods have very recently phosphorus, making wastewater and its accompanying solid shown great promise (Fig. 3C).28,29 fractions prime candidates for nutrient recovery, especially as a All of the above sustainable methods for the generation of lot of the necessary infrastructure is already in place. This article is licensed under a phosphorus-containing fine chemicals still rely on the thermal Wastewater is generally treated in wastewater treatment plants (WWTPs), where phosphate can be recovered from process for the initial conversion of PR to P4. Recently, Geeson and Cummins found a way to circumnavigate this prerequisite, multiple sources: aqueous streams (untreated wastewater, and showed that such organophosphorus compounds could be urine, effluent of treatment), sewage sludge, or sewage sludge Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. prepared from phosphoric acid derivatives. They showed that ash (SSA). Furthermore, there are alternative sources of phos- the trimetaphosphate salt, prepared from the dehydration of phate, including manure, slaughter waste and steelmaking phosphoric acid using sodium chloride, could be reduced to slag. All of these various sources will be examined in more À detail, and the nature of the recovered products for further use the novel bis(trichlorosilyl)phosphide anion, [P(SiCl3)2] , using trichlorosilane (Fig. 3D).30 This anion offered access to com- will be highlighted where appropriate. We have included a pounds including primary and secondary alkyl phosphines, selection of real-world industrial processes to showcase what which can be converted to organophosphinates and other is already being carried out and the challenges that remain in building blocks for pharmaceuticals. In a subsequent report, ensuring a fully circular phosphorus industry. À the dehydration step was eliminated, and the same [P(SiCl3)2] anion could be accessed directly from phosphoric acid and Phosphorus removal at wastewater treatment plants (WWTPs) 31 À trichlorosilane. In this case, isolation of the pure [P(SiCl3)2] There are several different forms in which phosphorus can anion was not possible, but it could be generated in situ and occur in wastewater. For example, wastewater from the animal reacted further to an organophosphorus derivative. These and livestock sector generally contains large amounts of studies show that it really is possible to completely bypass organic phosphates like phytic acid, a predominant form of the use of white phosphorus in the synthesis of useful organo- phosphate in monogastric animal manure. When looking at 32 3À phosphorus compounds, and it will be interesting to see if domestic wastewater, however, orthophosphate (PO4 ) is the these can be developed into useful industrial processes. It is most abundant. As this represents a far larger stream in terms worth noting that the industrial process to produce trichlor- of volume, most phosphate removal and recovery techniques osilane involves the use of elemental silicon, and elemental have focused on removing orthophosphate over other phos-

silicon requires similar amounts of energy to produce as white phate derivatives. It is worth noting that phosphine gas (PH3)

phosphorus, although recent studies have shown that SiCl4 has been observed in sewage sludge, where microorganisms are

92 | Chem. Soc. Rev.,2021,50,87--101 This journal is © The Royal Society of Chemistry 2021 View Article Online Chem Soc Rev Tutorial Review

able to produce this gas under anaerobic conditions.37 This is Phosphorus recovery at WWTPs especially pertinent given the recent use of phosphine gas as a As the paradigm regarding wastewater handling is slowly but 38 potential biomarker in the atmosphere of Venus. surely shifting from nutrient removal towards resource recovery Since the issue of eutrophication has been known for a long and recycling, other more bioavailable precipitates from the time, the development of technologies aimed at reducing the aqueous phase based on magnesium and calcium have started concentration of phosphorus in WWTP effluent started as early to gain interest. This section will discuss recovery of various as the 1950s. Two predominant technologies emerged which phosphates from the aqueous phase, sewage sludge, and the have since seen global implementation: the chemical precipita- incinerated form of the latter, sewage sludge ash. All discussed tion of metal phosphates and enhanced biological phosphorus technologies are represented in Fig. 4. 39 removal. Aqueous phase. Without prior concentration of P using Chemical precipitation. Metal phosphate precipitation is a EBPR, only about 10–40% P can be recovered from the aqueous straightforward technology based on the addition of iron or phase, depending on P already being bound to other metals or aluminium salts in the form of chlorides or sulfates, forming biomass. Furthermore, the liquid phase should have a phos- insoluble phosphate salts which can be removed after sedi- phate concentration of at least 50–60 mg LÀ1 for recovery to be mentation (for the solubility constants of relevant phosphate salts, economically viable, depending on the method employed.41 39 seeTableS1intheESI†). As a simple technique, it can be applied More importantly, however, constituent ions need to be present at various stages in the wastewater treatment process. Primary in sufficiently high concentrations for precipitation to occur at precipitation entails the addition of chemicals before sedimenta- all, and P concentrations of 100 mg LÀ1 are mentioned for tion, and the precipitate ends up in the primary sludge. Secondary effective precipitation of specific magnesium phosphate salts.42 precipitation is where the iron or aluminium salts are directly As these numbers are exceptionally high for untreated waste- added into the aeration tank of an activated sludge process, with water, the P-rich reject liquid phase of EBPR anaerobic treatment the phosphorus consequently ending up in the secondary sludge. is generally used for the precipitation processes from the aqueous

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. The third option is adding the flocculant post-sludge treatment, phase discussed herein. producing a relatively pure tertiary metal phosphate sludge. Due to Struvite. Struvite is a salt consisting of equimolar amounts

the costs of handling an additional stream however, this has of magnesium, ammonium and phosphate (MgNH4PO4Á6H2O). historically not been the method of choice. Nowadays, struvite is hailed as a promising way to recover Enhanced biological phosphorus removal (EBPR). As the phosphorus from wastewater, but initial reports were not as name implies, EBPR does not involve chemical dosing but positive; it was found as mineral encrustations inside digester instead relies on microorganisms to remove P from wastewater pipelines, reducing flow throughput and necessitating costly and is also widely used in WWTPs. The workhorses of this maintenance and downtime to remove. Indeed, when constitu- technology are a specific type of microbe, collectively named ent ions are present in sufficiently high concentrations and This article is licensed under a polyphosphate accumulating organisms (PAOs). They can conditions are alkaline, struvite can spontaneously precipitate.43 sequester phosphate as intracellular polyphosphate in excess As such, the controlled precipitation of struvite has gained interest, of their biological need under aerobic conditions, also dubbed serving two purposes: the omittance of costly maintenance and the ‘‘luxury uptake’’. More than 90% of the phosphorus present in recovery of phosphate. A significant added benefit is the simulta- Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. the wastewater can be removed this way, and where normal neous removal of ammonium from the wastewater. sludge biomass usually contains about 2–3% of phosphorus, Struvite precipitation processes are the most widely imple- reports have been made of P-contents ranging from 4% up to mented of the commercialised P recovery techniques, partly 12% post-EBPR.40 By subsequent removal of the sludge, net P due to their simplicity. A representative example is the Belgian removal from the wastewater is achieved. Part of the sludge is NuReSys (Nutrient Recovery Systems) process. The P-rich efflu- recirculated back to the aerobic tank where the process starts ent from EBPR anaerobic treatment is fed into a stirred tank over. When applying subsequent anaerobic conditions however, reactor, where magnesium is added in the form of soluble

the polyphosphates are released back into the solution as ortho- MgCl2 to achieve an equimolar Mg : P ratio. The pH is subse- phosphate allowing for an effective concentration of P in the liquid quently elevated to 8–9 using NaOH, at which point struvite phase. This is imperative for phosphorusrecoveryfromthe crystals start to form. The process is capable of reaching 90% aqueous phase to be viable. recovery of the P fed into the reactor.44 However only up to 40% Both chemical precipitation and EBPR are effective in the of the P in the WWTP can be harvested this way; the remaining removal of phosphorus from wastewater. However, the P 460% is lost to the sludge, where its reduced concentration removed is generally contained in the waste sludge and not hampers attempts to recycle this remaining part. Struvite finds valorised other than incidentally being applied to agricultural application as slow-release fertilizer, but as produced amounts land, or otherwise incinerated. The latter sees more and more increase, large scale applications are still missing. implementation in a number of European countries, following Calcium phosphate. Calcium phosphate recovery is also a concerns over spreading of drug residues, heavy metals and straightforward process, although it has been less widely

pathogens onto arable land via the sludge. Furthermore, FePO4 implemented than the analogous magnesium process. The

and AlPO4 lack proper bioavailability and consequently have most prominent example is the original DHV Crystalactor lower or little nutritional value depending on soil type. process.45 It uses a fluidized bed reactor with suitable seed

This journal is © The Royal Society of Chemistry 2021 Chem. Soc. Rev.,2021,50,87--101 | 93 View Article Online Tutorial Review Chem Soc Rev Creative Commons Attribution-NonCommercial 3.0 Unported Licence. This article is licensed under a Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM.

Fig. 4 Schematic overview of P recovery processes.

material, generally quartz. Ca(OH)2 is added as precipitating released by heating the sludge at 70 1C for 1 hour. The poly-P is

agent, after which calcium phosphate precipitates at a pH of 9. easily precipitated by subsequent CaCl2 addition. A marked Calcium phosphate can be used as slow-release fertilizer or as advantage over other precipitation processes is that elevated pH feedstock for regular fertilizer production. However, Crystal- is not necessary, reducing necessary chemicals. After calcina- actor units for phosphate recovery have not seen large imple- tion, the calcium poly-P can be mixed into the traditional wet mentation beyond the food industry due to economic reasons. process for phosphoric acid production.11 Interestingly, calcium polyphosphates can also be the target Iron phosphate. Another promising metal phosphate for P recovered material, which is the case in the Heatphos process. recovery is vivianite (iron(II) phosphate). Ferric iron (Fe(III)) Here, instead of applying anaerobic conditions to release is much more common under ambient conditions due to the orthophosphate during EBPR treatment, polyphosphates are presence of oxygen, however, vivianite forms readily under

94 | Chem. Soc. Rev.,2021,50,87--101 This journal is © The Royal Society of Chemistry 2021 View Article Online Chem Soc Rev Tutorial Review

reducing conditions. This can be induced under anaerobic quality requirements, and can be achieved in various ways. digestion conditions, where microorganisms also responsible A good example is the Stuttgart process,11 which has been for biogas formation can reduce Fe3+ to Fe2+. Other key factors operational as a large-scale test plant over the previous decade are the pH and sulfate concentrations, both due to competing at the WWTP Offenburg, Germany. P is leached from the sludge reactions. Neutral pH (6.0–8.0) is preferred, as more alkaline using sulfuric acid (pH E 3). To safeguard the quality of the

conditions will start to favour the formation of Fe(OH)2, precipitated struvite, citric acid is added as complexing agent whereas acidic conditions will simply dissolve the salt. prior to MgO and NaOH addition, and the resulting metal The vivianite can be separated from the sludge using a citrate salts stay in solution during struvite precipitation. magnetic separation process. Although there is a recent A process developed by Budenheim in Germany uses leaching increase in research into vivianite, it remains an iron phos- of phosphate from sludge by carbonic acid under pressure, phate which is not directly compatible with the mainstream followed by precipitation as calcium phosphate. fertilizer industry; more research is required for this to become The P recovery potential for these processes depends a widespread strategy in industry.46 Kemira’s Vivimag process strongly on process conditions like leaching pH and P specia- aims to leach phosphate from vivianite, to yield a fertilizer tion in the sludge. In the case of the Stuttgart process, recovery precursor and iron salts for re-use in wastewater treatment. values of 50 and 80% are reported for sludge with prior Sewage sludge. More than 30 million tons of sewage sludge phosphate precipitation using Al or Fe salts, respectively. is produced per annum in developed countries alone. As stated An overall recovery rate of 65% is reported by Egle and earlier, about 90% of influent P at WWTPs can be incorporated co-workers.48 in digested sludge. It is one the most concentrated forms of Thermochemical treatment of sewage sludge. Many processes phosphorus in organic waste streams, second only to bone for sewage sludge treatment make use of elevated temperatures, meal. There are currently a number of ways to dispose of and a range of different processes are employed. These can be the sludge: co-incineration in the cement industry, landfill, generally classified as hydrothermal treatment, pyrolysis and

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. agricultural use, or (mono)incineration, which provide oppor- gasification. The processes are typically differentiated by the tunities for more sustainable P recovery and recycling. The temperature used and the amount of oxygen present, as repre- cement industry uses sewage sludge as fuel in clinker production, sented in Fig. 4 (see also Table S2 in the ESI†). which leads the P contained therein to become locked and diluted Harsher temperature and higher oxygen profiles tend to incement.Actually,itspresenceis undesired for cement quality. achieve satisfactory depollution in terms of pathogens and Landfill is practised in all European countries to varying degrees. organics, but inorganic metal- and metalloid contaminants The disadvantages to this method are the evolution of methane, generally persist throughout these types of treatment, and a powerful greenhouse gas, and the increasing associated costs as exceed limits set for fertilizers and soil improvers as stated in available land becomes scarcer. Agricultural use utilizes the large the EU Fertilizing Products Regulation.49 Based on these con- This article is licensed under a amounts of nitrogen, phosphorus and potassium nutrients as well siderations, materials obtained from pyrolyzed and gasified as the organic matter present in the sludge. However, contami- sewage sludge appear to have limited potential on the fertiliser nants like heavy metals, pharmaceuticals, and pathogens are also market, and require further treatment. The described thermal prevalent, and these latter considerations have been the main treatments are, however, suitable to process a range of less Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. argument for countries which have implemented legislation contaminated materials like manure, bones, and food waste. limiting or outright banning the use of sewage sludge in None of these (hydro)thermal processes have seen widespread agriculture. Some countries where such legislation is in place, implementation yet. like the Netherlands, Switzerland, and increasingly Germany, have Sewage sludge ash (SSA). Incineration of sewage sludge to opted for the alternative option of incineration. This exothermic afford SSA reduces the volume by more than 90%, and the ashes process yields highly P-rich ashes, which are discussed in a have a P-content between 9–13.1%.50 Furthermore, organic patho- subsequent section.47 For the direct recovery of P from sewage gens and pharmaceutical contaminants are destroyed in the sludge, a multitude of technologies have been proposed, some of process, and the fact that SSA is a dry and free-flowing powder which have seen real-world implementation. We can divide these makes subsequent handling relatively easy. The main downside of in wet-chemical leaching and thermal technologies, related to the sewage sludge incineration is the fact that large infrastructural beneficiation of PR. investments for incineration facilities are needed, even though Wet-chemical treatment of sewage sludge. This process benefits of economy of scale and centralization can mitigate this. involves the release of P into solution by first treating the It is highly unlikely countries will invest in these practices for the sludge with a mineral acid. Wet-chemical leaching technologies sake of P recovery alone, especially in areas where the application build on the previously discussed precipitation technologies, of sewage sludge to arable land is still practised. However, the however the acidic leaching inevitably co-solubilizes heavy process becomes more attractive when the direct use of sewage metals also present in the sludge and potentially large amounts sludge has been banned altogether, like in Switzerland and the of iron and/or aluminium depending on whether metal phos- Netherlands,whereallthesewagesludgeismono-incinerated. phate precipitation was initially employed to remove P from Currently, these ashes are often incorporated in cement or asphalt the liquid phase. The omittance of metal incorporation is or simply sent to landfill, effectively wasting valuable resources, as imperative for recovered materials to meet legislative and about 87% of the P in WWTP influent persists in SSA.48

This journal is © The Royal Society of Chemistry 2021 Chem. Soc. Rev.,2021,50,87--101 | 95 View Article Online Tutorial Review Chem Soc Rev

Many of the metals present are non-volatile at the employed ash forms carbonic acid, which can react with the phosphate in temperatures and conditions. As such, the large reduction the ash to form phosphoric acid. A less widely utilised alternative in volume also means that heavy metals become more concen- to acidic wet-chemical treatment is the alkaline counterpart. The trated. This, in combination with low reported bioavailability alkaline leaching is practised on an industrial scale in Gifu, Japan, of the present P-species exclude the option of using SSA directly by treating SSA with hydroxide solutions. The leached ashes are

as fertilizer. Consequently, valorisation of the ashes is needed washed and subsequently treated with a dilute H2SO4 solution, to recover P in a usable form, and various technologies which removes the toxic heavy metals. The resulting solids can be have been developed to this end. By direct analogy with the used in cement, asphalt, as roadbed material or as soil improver. treatment of sewage sludge, the methodologies for treating SSA The P extraction rate is strongly dependent on the calcium (CaO) can be divided into wet-chemical processes and thermochemi- content in the ashes, and overall a P recovery of 30–40% is cal processes. reported, much lower than acidic treatment processes. Chemical Wet-chemical treatment of SSA. The majority of SSA valor- costs are also significant due to the large amounts of chemicals isation technologies employ wet-chemical treatment, which are needed. On the other hand, the method does remove a lot of the either based on acidic or alkaline leaching. Acidic leaching heavy metal contaminants, and whileitisnotthemostefficient is quite similar to previously discussed processes involving process in terms of P recovery, it is fully operational and has been acid digestion, and is the most frequent technique seen for supplyinglocalfarmerswithover300tyÀ1 of recovered fertilizer SSA treatment. Different acids can be employed in this since 2009.11 Economics depend on the local availability of caustic process, including sulfuric acid, hydrochloric acid, phosphoric soda waste, which is relatively expensive when bought at the acid, and carbonic acid, and some of these processes will be market. highlighted below. Thermochemical treatment of SSA. The thermochemical The traditional wet phosphoric acid process discussed treatment of SSA involves reacting the ash with dosed chemicals earlier is in essence an acidic wet-chemical treatment. As SSA at elevated temperatures. The main goals of this are to remove

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. has such a high P-content, both ICL in the Netherlands and heavy metal contaminants and increase the bioavailability of P. Nippon Phosphoric Acid Co. Ltd (NPA) in Japan started trials A key example of this is Outotec’s AshDec process, on which mixing in ashes with PR to feed their production facilities in research started back in 2004 in Germany and Switzerland.11 the hopes of integrating this secondary feedstock into existing In this process, ashes are fed into a rotary kiln dosed with sodium, infrastructure and this has been reasonably successful. NPA magnesium or potassium salts and a reducing agent, preferably was able to use a blend ratio of up to 2.5% SSA without dry sewage sludge, and heated to 900–950 1C for 15–20 minutes. significantly affecting plant performance, product quality and Ideally, the ash is taken directly from an adjacent incineration pollution levels. After acquiring the necessary industrial waste reactor, reducing energy requirementsastheashesarestillhot. disposal business licence, mixing practices were implemented The system ensures heavy metal removal by volatilization in a

This article is licensed under a À1 commercially in 2013, accepting about 1300 t y of SSA from reducing atmosphere, giving bioavailable CaKPO4 and CaNaPO4 local sludge incineration facilities. The main issue with this compounds as products. Copper and zinc, the most common practice is the fact that the relatively large amounts of heavy heavy metals in SSA, are removed to a large extent and the product metals present in SSA are incorporated in the fertilizer product. meets fertilizer regulations. Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. ICL blends SSA into its TSP (solid fertilizer) production, with For more extensive metal removal, for example in the case of

the advantage that the ash does not pass through a truly liquid high copper concentrations, inorganic chlorides like MgCl2 or phase preventing excessive metal solubilisation. Metal contami- CaCl2 can be added to generate volatile metal chlorides, in this 11 nation starts to become a real issue for blends above 2.5% SSA, case CuCl2. The downside of this practice is that the formed

and technologies to remove metals from phosphoric acid solutions chlorapatite (Ca5(PO4)3Cl1Àx(OH)x) has low overall bioavailability,

have not been implemented due to economic considerations. and farringtonite (Mg3(PO4)2)andstanfieldite(Ca4Mg5(PO4)6) As such, SSA originating from WWTPs employing chemical only show agronomic efficiency in acidic soils. Interestingly, the precipitation with iron and/or aluminium is less suited for blending AshDec technology was initially based on the use of chlorides due than that of WWTPs employing biological P removal.11 to more stringent regulations on recycled fertilizers in place in Straight acid digestion of the ash with mineral acids is also Germany (until 2008) and Switzerland (until 2017). As more possible. The TetraPhos process (Remondis) leaches phosphate accessible limit values became the norm, the process switched from the ash by means of phosphoric acid, which is then to additives allowing for more bioavailable products. One down- treated with sulfuric acid to give phosphoric acid, and acting side of the technology is its large energy consumption, but a as the ultimate source of the acid. The EcoPhos process, sold to significantbenefitisthefactthatitisnotlimitedtotheuseofSSA Prayon after EcoPhos went bankrupt, uses HCl digestion on the as feedstock, but is compatible with other P-rich ashes as well, as ash followed by precipitation of the phosphate with lime to give aredescribedinthefollowingsection. dicalcium phosphate. The remaining calcium chloride can be White phosphorus can be produced from SSA in a classical

disposed of at sea, while heavy metals remain with the insoluble P4 furnace, however Fe levels need to be limited to prevent the residue or are removed by ion exchange. formation of excessive amounts of a less valuable by-product,

Another method of acidic treatment is the use of CO2 instead ferrophosphorus. This limits suitable ashes to WWTP sludges

of mineral acids. Blowing CO2 into an aqueous suspension of the with Al precipitation and EBPR as P removal technology. A new

96 | Chem. Soc. Rev.,2021,50,87--101 This journal is © The Royal Society of Chemistry 2021 View Article Online Chem Soc Rev Tutorial Review

process indicating to bypass the iron issue was developed By using MBM in cement works, the P ends up diluted and by the RecoPhos consortium, a technology now acquired by locked in concrete. When mono-incinerated, still a rare practice

Italmatch, which uses an inductively heated coke bed to in Europe, the ashes (MBMA) mostly comprise Ca5(PO4)3OH

reduce SSA. and Ca3(PO4)2, and have a composition closely reminiscent to that of PR, exhibiting P contents as high as 15–19% with similar Alternative phosphorus sources or lower heavy metal content.54 As such, MBMA is a prime While we have so far focused mostly on P recovery from waste- candidate for P recycling, and there are numerous ways to water, there are a number of alternative waste streams from valorize the P content in these ashes. The most straightforward which phosphate can be recovered and utilised. These are is acidic leaching, similar to the wet-chemical methods mostly animal-derived waste streams. First and foremost, live- handled in previous sections. Extensive pilots have been con- stock manure represents a large waste stream rich in P. In fact, ducted by ICL mixing MBMA into existing (wet) processes based with 1.6 Mt P per year, it is the largest source of recyclable P in on PR, yielding good results.11 Furthermore, P valorization Europe.36 It is a much more localized stream compared to technologies applicable to SSA can be extended to MBMA, with municipal wastewater. In most countries, manure is simply the latter exhibiting better properties in terms of P content and applied to land as organic fertilizer. However, countries with heavy metal contaminants. dense livestock industries like the Netherlands and Belgium Another waste stream of interest is steelmaking slag.11 The generate large volumes of manure, but arable land to apply it to raw materials of steelmaking (iron ore, CaO, and coal) do not is limited. As such, the risk of manure overapplication in these contain much phosphorus (0.05–0.06 wt%), but the impurities livestock-intensive regions is a real problem, both in terms of are concentrated in the steel production process and end up nutrient loading as well as the accumulation of contaminants unevenly distributed in the slag. Phosphorus has a negative present in the manure. Consequently, other ways of disposal impact on the quality of steel and is therefore actively removed. are warranted, provided this type of livestock-intensive agri- Since steel production is one of the larger industrial processes

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. culture persists. The transportation of excess manure to other worldwide, this results in vast amounts of slag with concen- areas presents a logistical challenge, as it is a bulky (water-rich) trated levels of phosphorus compared to its parent raw material substance and therefore highly unfavourable to move around (0.3–1.7 wt%). Multiple techniques have been proposed for from an economic perspective, especially over longer P recovery from steelmaking slag. These include magnetic distances.51 Local treatment is therefore warranted, and there separation, capillary action separation, aqueous dissolution are numerous options to this end. Oftentimes, the first manure and carbothermic reduction, as well as reductive melting. treatment step is anaerobic digestion, producing valuable While the latter has been run at pilot-scale,11 currently it is biogas (methane). This can be applied to wet manure, but more not economically attractive to actively use steelmaking slag as a generally its dewatered counterpart. This is also the case for source of phosphorus. However, with the projected increase of This article is licensed under a thermal treatments like wet oxidation (hydrothermal), pyrolysis PR pricing accompanying its depletion, this could become and gasification. However, these are merely volume reductions feasible in the future. to make transport less expensive, and do not address the local oversupply of P, which remains in the digestate. Alternatively, Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. follow-up treatments of the resulting biochar as discussed in Closing the loop: drivers and barriers the section on sewage sludge thermal treatment can also be for recycling applied. Similarly, the incineration of manure is also an option, recovering its energy content at the expense of C- and N-based The principal initial driver for P recovery was not so much nutrients. The ashes can be treated by analogous methods to focused on the recovery of P in a usable form, but rather its the SSA, although this practice would also require significant removal from wastewater to prevent pollution. Legislation has infrastructural investments. Furthermore, the resulting liquid frac- therefore been put into place in many developed countries, tion from dewatering can be used for the precipitation of calcium spurring the widespread implementation of chemical precipi- phosphate or struvite. This only contains up to 30% of the total P tation and biological treatment systems to treat wastewater and however, and may not be economically viable in all cases.52 counter the harmful phenomenon of eutrophication. Nowadays, Another large P-containing waste stream is Category I meat many WWTPs still employ either, or even both, but the resulting and bone meal (MBM). MBM is a by-product of the rendering of P-rich materials have seen only little reintroduction in the P animals and is rich in a range of nutrients. Historically, MBM cycle. Over the last couple of decades, however, P-rich streams was generally processed towards animal feed, but due to like wastewater are increasingly seen as promising secondary the BSE (bovine spongiform encephalopathy, or ‘‘mad cow resources of P, emphasizing the need for its recovery in usable, disease’’) crisis this practice was partially banned in the EU. bioavailable form; the focus is shifting from P removal to While legislation was softened somewhat a number of years P recovery and recycling. This shift is exacerbated by the later, large amounts of MBM still need to be disposed of, with increasingly pronounced public opinion on sustainability and MBM production exceeding 3.5 million tons per year in the circularity, and the need for it is underlined by the inclusion of 53 EU. Since then, MBM is often incinerated to valorise its PR (as well as P4) on the list of critical raw materials as energy content in cement works, and destroy any pathogens. formulated by the European Commission.

This journal is © The Royal Society of Chemistry 2021 Chem. Soc. Rev.,2021,50,87--101 | 97 View Article Online Tutorial Review Chem Soc Rev

The uneven distribution of PR reserves has led to a lot of by-products, struvite, biochar, sewage sludge and its derivative countries being highly dependent on imports and consequently ashes. When quality requirements are fulfilled, outputs have subject to price fluctuations of the resource. In 2008, an product status and are no longerconsideredwaste,removing extreme fluctuation occurred, driving up PR prices from about legal hurdles and promoting marketing of these materials. While $50 tÀ1 a year earlier to $430 tÀ1,55 which in turn was largely these requirements will still be stringent, legislation on waste responsible for sharp increases in food prices worldwide. status has finally been harmonized, facilitating more facile free Having a local, sustainable, and virtually inexhaustible source trade of CMC materials. Another important change is the intro- of renewable fertilizer would alleviate these issues to a large duction of a Cd limit on fertilizer. A maximum of 60 mg Cd per kg

extent by decoupling food production from foreign and fossil P2O5 is now mandatory. As virgin mineral fertilizers generally resources. Much effort has gone into the development of P contain significantly higher Cd concentrations than recovered recovery technologies and significant progress has been made, materials, this gives recycled material an advantage.57 However, as highlighted in this review. Still, commercially operating having a facilitating legal framework in place is not enough. processes are not abundant, and most of them are based on As noted for struvite, an economic driver is needed for P recovery struvite precipitation. The relative success of struvite can be technologies to become more widely implemented, which explained by the fact that its removal addresses another issue: naturally extends to P recycling practices. that of unwanted precipitant scaling in biological wastewater A paramount driving force towards P recycling would be to treatment piping. By removing the struvite in a controlled ban recovered P from going anywhere but a true recycling manner, costly maintenance can be prevented, which provides an operation. As is clear from the technology review, the economics additional economic incentive for targeted struvite precipitation. of P recovery are often weak, due to a number of factors (economy There is however a distinction to be made between P of scale, technological complications), hence blocking routes recovery and P recycling, and their associated drivers. The leading to P wastage in e.g. landfill, asphalt fillers, etc. is seen as reasons for the relative success of struvite are very much based themosteffectivewaytocreateatruePcycle.Thebanon

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. on incentives for P recovery: the mandatory P removal from agricultural spreading of sewagesludgeintheNetherlands, wastewater under the Wastewater Directive from a legislative Switzerland and parts of Germany has already helped in creating perspective, and the prevention of maintenance costs from an an infrastructure which makes large amounts of SSA available; the economic standpoint. A good example of driving P recovery is legislation enforcing P recycling until 2026 as now seen in the relatively stringent legislation in place in Switzerland since Germany will make many technologies with marginal economics 2016 and Germany since 2017. Germany and Switzerland have more viable. since taken a leading role in the speed and degree of imple- mentation of P recovery technologies compared to other Eur- Value chains opean nations. Indeed, environmental regulations have always We cannot escape the need for economic viability. The P This article is licensed under a been a key driver for sustainable innovation. However, while recycling sector will never truly thrive if there is no prospect this progress is to be applauded, it only solves part of the of financial gain; something that cannot sustain itself will never puzzle; P recycling, by using recovered P as resource for the truly contribute to sustainability, irrespective of how well the production of marketable products, is needed to truly close the people and planet have been integrated into the concept. Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. loop. To this end, recovery and recycling need to be aligned to A value chain is needed to close the loop, where recovery serves make sure the recovered material is suitable for subsequent as supply and recycling as demand (Fig. 5). recycling, and value chains are needed to bridge the gap There are many stakeholders involved in the secondary between them.11 fertilizer industry, including governmental bodies, WWTPs, P valorisation companies, farmers and the general public. Effec- Legislation tive sales of a product rely on criteria on which stakeholders Legislation is a key factor in the promotion of P recycling. One should be in alignment. This way, the (prospective) added value issue from a legislative standpoint is that recovered materials of a particular recovered material can be determined, which is are designated as waste. A waste material may only be moved necessary to close the gap. Examples are nutrient content, across borders following a lengthy process involving written homogeneity of the material, purity, proof of agronomic effi- notifications and authorization in accordance with the Ship- ciency and guarantees for sufficient quantities. Without them, ment of Waste Regulation,56 which has further hampered the a secondary fertilizer will intrinsically be of lower value or even development of a European sustainable P market. The EU has lose all interest, and a value chain might not be established.11 undertaken action to facilitate the use of recovered materials, by Achieving such alignment is challenging, but there are inter- revising the Waste Framework Directive in 2018 and Fertilizers organizational platforms and international studies whose main Regulation in 2019 as part of the Circular Economy Package goals are to facilitate this. A prime example is the European launched in 2015.57 The new EU Fertilizing Product Regulation Sustainable Phosphorus Platform (ESPP), which comprises over introduces product function categories (PFC) regarding materials 150 members stemming from various stakeholder groups in to be used as fertilizer, and component material categories (CMC) industry, science and policy. Its main goal is to promote which encompass raw materials for fertilizer production. The P sustainability in Europe by identifying and addressing latter is expanded to now include compost, digestates, animal obstacles and facilitate opportunities like collaborative actions,

98 | Chem. Soc. Rev.,2021,50,87--101 This journal is © The Royal Society of Chemistry 2021 View Article Online Chem Soc Rev Tutorial Review

Outlook The interplay between stakeholders, recovery and recycling strategies and associated legislation is paramount for enabling secondary fertilizers to penetrate the market. Still, even in a hypothetical perfect case where all stakeholders are aligned, all legislation is adhered to and the value chain is in place, the market may still not favour secondary fertilizers over virgin ones simply due to competition. It has been postulated that for P recovery and recycling from wastewater to become truly self-sufficient, PR prices need to be at least 100 $US tÀ1.58 As of March 2020, prices were just above 70 $US tÀ1 (for Moroccan PR) and have been steadily declining over the last few years.55 Indeed, the low price of PR has to date been a key barrier for the implementation of P recovery systems. Still, despite this recent decline, prices are significantly higher now than they were before the price spike of 2008 and are expected to rise in the future as increasingly contaminated PR pushes mining and beneficiation costs. In time, this economic barrier is expected Fig. 5 Necessity of a value chain to close the gap between supply and to become a driver, and value chains should be in place to demand. capitalize on it when that happens. Analogously, production of more specialized, higher value P compounds from secondary sources could also start to become more viable. This may well

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. business cases and the establishment of value chains. The prove to be a very interesting emerging market when recovered Dutch Nutrient Platform in the Netherlands strives towards P materials start taking precedence over PR. It is expected that the same goals on a national level. In 2011, they initiated the anywhere between 17 to 31% of P currently derived from fossil Phosphorus Value Chain Agreement, bringing together twenty resources can be substituted in Europe by use of recycled 11 parties to further a sustainable market for P recycling. The materials in a fully-fledged market.49 A promising prospect recently published STRUBIAS report explored the technical and indeed! market conditions for using products derived from biogenic waste or other secondary raw materials as fertilizers, and showed that the agronomic efficiency of secondary fertilizers Conclusions This article is licensed under a is generally in line with their PR-derived counterparts.49 Another important facet of stakeholder alignment in which This review is an introductory text into the complex and wide- these facilitating bodies play a role is educating the customer ranging topic of phosphorus recovery and recycling. It is segment and raising general awareness; primarily, the way as important to change the way we deal with phosphorus and Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. to how recovered fertilizing materials are perceived by the close the loop. The requirement for cheap chemical conver- market.11 In regions where there is some supply of recovered sions from renewable phosphate resources to highly pure fertilizer like struvite or calcium phosphates, farmers have to phosphorus-containing building blocks is imperative, and date been reluctant to switch from traditional mineral fertili- recycling schemes should be implemented rapidly. Chemical zers to its recovered counterpart. This is understandable, as the pathways should be assessed over the full cycle for effective latter are predominantly slow-release fertilizers in contrast to recovery and effective recycling to usable products. Other the highly soluble ammonium- and potassium phosphates factors that make a process industrially viable are often over- commonly used. Therefore, it is most desirable to produce looked, and phosphate rock is currently still a relatively cheap known products, but using renewable resources. An example resource. The factors that need to be considered for new of the importance of customer education is the calcium phos- recycling schemes to kick-start this process are politics, legislation, phate product produced by alkaline leaching of SSA in Gifu, societal pressure, and of course economics. Sustainability goals set Japan. Upon full-scale operation of the process, no channels by the government can be a political driver, but for fertiliser were in place for the sales of the material. To alleviate this issue producers and farmers, the ill-defined properties of recovery and establish a value chain, a marketing campaign was products such as struvite in comparison to established fertilisers launched including advertisements, briefing sessions for farm- form a barrier to adopting them. Social drivers are the popularity of ers, free sample offerings and leaflet distribution. Now, it is the circular economy and the green image for marketing. Water sold to local farmers and enjoys a good reputation, with sales boards are economically hindered by high investment costs and volumes increasing annually and serves as a good example of uncertainty of the return on investment for the implementation of how P recycling can be achieved on a local level.11 The chal- struvite recovery processes. The reduction in maintenance costs lenge now is to translate these relatively small-scale examples to however (prevention of blocking of pipes) is a strong driver. an international market. Scientists, policymakers and companies are on the right track to

This journal is © The Royal Society of Chemistry 2021 Chem. Soc. Rev.,2021,50,87--101 | 99 View Article Online Tutorial Review Chem Soc Rev

effectively recover and recycle phosphorus. They are learning to 15 K. Schro¨dter,G.Bettermann,T.Staffel,F.Wahl,T.Kleinand deal with new raw materials from waste, a myriad of recovery and T. Hofmann, Ullmann’s Encyclopedia of Industrial Chemistry, recycling schemes and a great deal of uncertainty. By aligning such Wiley, Weinheim, Germany, 2008. stakeholders, barriers can be mitigated and drivers exploited/ 16 H. Von Plessen and G. Schimmel, Chem. Ing. Tech., 1987, 59, amplified, allowing the establishment of value chains to become 772–778. easier and thus more likely. These will prove imperative in moving 17 B. M. Cossairt, M. C. Diawara and C. C. Cummins, Science, away from fossil feedstocks, and towards renewable ones, and help 2009, 323, 602. to close the loop of the phosphorus cycle. 18 A. R. Jupp and D. W. Stephan, Trends Chem., 2019, 1, 35–48 and references within. 19 R. Engel, Synthesis of Carbon-Phosphorus Bonds, CRC Press, Conflicts of interest 2nd edn, 2003. J. C. S. is co-founder, shareholder and scientific advisor of 20 N. Weferling, S. M. Zhang and C. H. Chiang, Procedia Eng., SusPhos BV. W. S. is CTO and shareholder of SusPhos BV. 2016, 138, 291–301. 21 J. L. Montchamp, Acc. Chem. Res., 2014, 47, 77–87. 22 E. D. Weil and S. V. Levchik, Flame Retardants for Plastics Acknowledgements and Textiles: Practical Applications, Carl Hanser Verlag, Munich, 2009, p. 97. Renske Verhulst (Dutch Nutrient Platform) and Aalke Lida de 23J.E.Borger,A.W.Ehlers,J.C.SlootwegandK.Lammertsma, Jong (AquaMinerals) are thanked for their feedback on a draft Chem. – Eur. J., 2017, 23, 11738–11746 and references within. of this manuscript. This work was supported by the Council for 24 G. Mu¨ller, M. Zalibera, G. Gescheidt, A. Rosenthal, Chemical Sciences of The Netherlands Organization for Scien- G. Santiso-Quinones, K. Dietliker and H. Gru¨tzmacher, tific Research (NWO/CW) by a VIDI grant (J. C. S.), and a VENI Macromol. Rapid Commun., 2015, 36, 553–557. grant (A. R. J.), a NWO KIEM GoChem grant with SusPhos BV

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. 25 N. N. Greenwood and A. Earnshaw, Chemistry of the Elements, (J. C. S.) and a CE-RUR-08-2018-2019-2020 grant LEX4BIO Butterworth-Heinemann, Boston, Mass., 2nd edn, 1997. (J. C. S., grant agreement no. 818309). 26 J. H. Clark and D. J. Macquarrie, Handbook of Green Chemistry and Technology, John Wiley & Sons, 2002. References 27 C. J. O’Brien, J. L. Tellez, Z. S. Nixon, L. J. Kang, A. L. Carter, S. R. Kunkel, K. C. Przeworski and G. A. Chass, Angew. 1 M. E. Weeks, J. Chem. Educ., 1933, 10, 302–306. Chem., Int. Ed., 2009, 48, 6836–6839. 2 J. Emsley, The 13th Element: The Sordid Tale of Murder, Fire, 28 J. S. Elias, C. Costentin and D. G. Nocera, J. Am. Chem. Soc., and Phosphorus, Wiley, New York, 2000. 2018, 140, 13711–13718. This article is licensed under a 3 I. Asimov, The Magazine of Fantasy and Science Fiction, 29 S. Manabe, C. M. Wong and C. S. Sevov, J. Am. Chem. Soc., Mercury Press, Oklahoma City, 1959. 2020, 142, 3024–3031. 4 G. M. Filippelli, Elements, 2008, 4, 89–95. 30 M.B.GeesonandC.C.Cummins,Science, 2018, 359, 1383–1385. 5 P. J. A. Withers, J. J. Elser, J. Hilton, H. Ohtake, 31 M. B. Geeson, P. Rı´os, W. J. Transue and C. C. Cummins, Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM. W. J. Schipper and K. C. van Dijk, Green Chem., 2015, 17, J. Am. Chem. Soc., 2019, 141, 6375–6384. 2087–2099. 32 M. B. Geeson and C. C. Cummins, ACS Cent. Sci., 2020, 6, 6 O. Gantner, W. Schipper and J. J. Weigand, in Sustainable 848–860. Phosphorus Management, ed. R. W. Scholz, A. H. Roy, 33 J. M. Roberts, J. L. Placke, D. V. Eldred and D. E. Katsoulis, F. S. Brand, D. T. Hellums and A. E. Ulrich, Springer, Ind. Eng. Chem. Res., 2017, 56, 11652–11655. Dordrecht, 2014, pp. 237–242. 34 J. C. Slootweg, Curr. Opin. Green Sustainable Chem., 2020, 23, 7 D. Cordell and S. White, Sustainability, 2011, 3, 2027–2049. 61–66. 8 S. J. van Kauwenbergh, World Phosphate Rock Reserves and 35 T. Keijer, V. Bakker and J. C. Slootweg, Nat. Chem., 2019, 11, Resources, 2010. 190–195. 9 M. Wang, C. Hu, B. B. Barnes, G. Mitchum, B. Lapointe and 36 K. C. van Dijk, J. P. Lesschen and O. Oenema, Sci. Total J. P. Montoya, Science, 2019, 365, 83–87. Environ., 2016, 542, 1078–1093. 10 J. Elser and E. Bennett, Nature, 2011, 478, 29–31. 37 I. De´vai, L. Felfo¨ldy, I. Wittner and S. Plo´sz, Nature, 1988, 11 H. Ohtake and S. Tsuneda, Phosphorus Recovery and Recy- 333, 343–345. cling, Springer, 2018 and references within. 38 J. S. Greaves, A. M. S. Richards, W. Bains, P. B. Rimmer, 12 J. C. Slootweg, Angew. Chem., Int. Ed., 2018, 57, 6386–6388. H. Sagawa, D. L. Clements, S. Seager, J. J. Petkowski, 13 H. Tayibi, M. Choura, F. A. Lopez, F. J. Alguacil and C. Sousa-Silva, S. Ranjan, E. Drabek-Maunder, H. J. Fraser, A. Lopez-Delgado, J. Environ. Manage., 2009, 90, 2377–2386. A. Cartwright, I. Mueller-Wodarg, Z. Zhan, P. Friberg, 14 V. N. Rychkov, E. V. Kirillov, S. V. Kirillov, V. S. I. Coulson, E. L. Lee and J. Hoge, Nat. Astronomy, 2020, Semenishchev, G. M. Bunkov, M. S. Botalov, D. V. DOI: 10.1038/s41550-020-1174-4. Smyshlyaev and A. S. Malyshev, J. Clean. Prod., 2018, 196, 39 G. Morse, S. Brett, J. Guy and J. Lester, Sci. Total Environ, 674–681. 1998, 212, 69–81.

100 | Chem. Soc. Rev.,2021,50,87--101 This journal is © The Royal Society of Chemistry 2021 View Article Online Chem Soc Rev Tutorial Review

40 P. H. Liao, W. T. Wong and K. V. Lo, J. Environ. Eng. Sci., precipitated phosphate salts & derivates, thermal oxidation 2005, 4, 77–81. materials & derivates and pyrolysis & gasification materials, 41 P. Cornel and C. Schaum, Water Sci. Technol., 2009, 59, Publications Office of the European Union, 2019. 1069–1076. 50 O. Kru¨ger, A. Grabner and C. Adam, Environ. Sci. Technol., 42 P. Kehrein, M. van Loosdrecht, P. Osseweijer, M. Garfı´, 2014, 48, 11811–11818. J. Dewulf and J. Posada, Environ. Sci.: Water Res. Technol., 51 P. J. A. Withers, K. C. van Dijk, T. S. S. Neset, T. Nesme, 2020, 6, 877–910. O. Oenema, G. H. Rubæk, O. F. Schoumans, B. Smit and 43 J. D. Doyle and S. A. Parsons, Water Res., 2002, 36, S. Pellerin, Ambio, 2015, 44, S193–S206. 3925–3940. 52 O. F. Schoumans, F. Bouraoui, C. Kabbe, O. Oenema and 44 E. Desmidt, K. Ghyselbrecht, Y. Zhang, L. Pinoy, B. Van der K. C. van Dijk, Ambio, 2015, 44, S180–S192. Bruggen, W. Verstraete, K. Rabaey and B. Meesschaert, Crit. 53 E. Cascarosa, G. Gea and J. Arauzo, Renewable Sustainable Rev. Environ. Sci. Technol., 2014, 45, 336–384. Energy Rev., 2012, 16, 942–957. 45 Crystalactor Water Technology by Royal HaskoningDHV, 54 M. Coutand, M. Cyr, E. Deydier, R. Guilet and P. Clastres, www.royalhaskoningdhv.com/en/crystalactor, (accessed 4 J. Hazard. Mater., 2008, 150, 522–532. July 2020). 55 Rock Phosphate - Monthly Price - Commodity Prices - Price 46 Y. Wu, J. Luo, Q. Zhang, M. Aleem, F. Fang, Z. Xue and Charts, Data, and News - IndexMundi, www.indexmundi. J. Cao, Chemosphere, 2019, 226, 246–258. com/commodities/?commodity=rock-phosphate&months=180, 47 H. Herzel, O. Kru¨ger, L. Hermann and C. Adam, Sci. Total accessed 4 July 2020. Environ, 2016, 542, 1136–1143. 56 S. Hukari, L. Hermann and A. Na¨ttorp, Sci. Total Environ, 48 L. Egle, H. Rechberger, J. Krampe and M. Zessner, Sci. Total 2016, 542, 1127–1135. Environ, 2016, 571, 522–542. 57 B. Garske, J. Stubenrauch and F. Ekardt, Review of European, 49 D. Huygens, H. Saveyn, D. Tonini, P. Eder and L. Delgado Comparative & International Environmental Law, 2020, 29,

Creative Commons Attribution-NonCommercial 3.0 Unported Licence. Sancho, Technical proposals for selected new fertilising 107–117. materials under the Fertilising Products Regulation 58 J. Von Horn and C. Sartorius, International Conference on (Regulation (EU) 2019/1009): process and quality criteria, Nutrient Recovery from Wastewater Streams Vancouver, IWA and assessment of environmental and market impacts for Publishing, London, 2009. This article is licensed under a Open Access Article. Published on 19 November 2020. Downloaded 9/25/2021 8:07:52 PM.

This journal is © The Royal Society of Chemistry 2021 Chem. Soc. Rev.,2021,50,87--101 | 101